Introduction
In order to grow, multiply, and transmit, pathogens obtain resources
from their host, and theoretically the resulting within-host infection
load is expected to be proportional to the gained resources. However,
too high rates of within-host infection load may come at the cost of
increased virulence, thereby incurring a cost for the pathogen as
decreased transmission (Blanquart et al., 2016). Thus, evolutionary
theory and experimental studies (de Roode et al., 2008) have established
that selection should favour intermediate levels of within-host
infection load. This trade-off between within-host infection load and
transmission has been proposed to maintain polymorphism in pathogen
populations, and to prevent the rise of highly virulent pathogens
(Frank, 1992). Trade-offs have been sought as an evolutionary solution
to limit disease epidemics and the emergence of pathogen strains with
extremely high within-host infection load (Zhan et al., 2015). However,
insight on how pathogen within-host infection load links to transmission
during epidemics where pathogens may encounter variation in both biotic
and abiotic conditions (Susi & Laine, 2013, Blanquart et al., 2016,
Dutta et al., 2021) has remained limited (Acevedo et al., 2019). In the
wild, the limited evidence for trade-offs may be explained by spatial
(Osnas et al., 2015) and host mediated processes (Kubinak et al., 2012).
The trade-offs restraining within-host infection load may also occur
between other traits i.e. adaptation to abiotic conditions (Mboup et
al., 2012) or be context-dependent and become evident in stressful
environments (Susi & Laine, 2013).
The drivers of disease evolution and epidemics are rarely limited to the
interplay of one host and one pathogen, as in the wild most infections
occur as coinfections whereby multiple pathogens are simultaneously
infecting the same host (Tollenaere et al., 2016, Telfer et al., 2010).
Coinfection may fundamentally change pathogen host exploitation strategy
in order to outcompete other pathogens sharing the same limited resource
(de Roode et al., 2005, Alizon et al., 2009, Alizon & van Baalen,
2008). Thus, it has been suggested that coinfection is an important
driver of disease evolution (Alizon & van Baalen, 2008, Alizon et al.,
2009). Experimental approaches have measured increased within-host
infection load(Bell et al., 2006) and transmission(Susi et al., 2015b,
Susi et al., 2015a) under coinfection but there are also exceptions to
this trend (Orton & Brown, 2016). Overall, it is well established that
the pathogen within-host infection load may change under coinfection,
but studies explicitly testing trade-offs between within-host infection
load and transmission under coinfection are rare, and evidence remains
mixed (Suffert et al., 2016, Sacristan & Garcia-Arenal, 2008).
Furthermore, experiments have often been conducted using strains of the
same pathogen species, although interspecific interactions among
pathogen species are likely to play an important role, as individual
hosts often support diverse pathogen assemblages(Susi et al., 2019,
Dallas et al., 2019, Telfer et al., 2010).
While intraspecific coinfection is a pre-requisite of outcrossing for
many pathogens (Suffert et al., 2016), theory predicts the intensity of
competition to increase as relatedness decreases (Alizon et al., 2013).
Across plants (Tollenaere et al., 2016, Tollenaere et al., 2017),
animals (Telfer et al., 2010) and humans (Lawn et al., 2006, Chen et
al., 2020) inter-kingdom coinfections are common, and they are often
suggested to have serious consequences in disease epidemics and disease
severity. In particular, it is becoming increasingly clear that viruses
are ubiquitous in nature (Munson-McGee et al., 2018, Bernardo et al.,
2017), although their true diversity and prevalence in natural
populations has been under-estimated for a long time (Wren et al., 2006,
Roossinck et al., 2015). The ecological roles of viruses are still
poorly understood (Roossinck, 2010, Alexander et al., 2014), but they
have the potential to interact with other pathogen species via
competition for shared host resources, and via shared effects on host
immunity (Huang et al., 2019, Uehling et al., 2017). Thus, it is vital
to test how coinfection with pathogens from distant taxa may influence
within-host infection load and transmission and their potential
trade-offs.
Phomopsis subordinaria is a castrating pathogen that infects its
hosts through seed stalks. Here, we investigate trade-offs between
within-host infection load and transmission by surveying 260 host plant
(Plantago lanceolata ) populations in the Åland Islands,
south-west Finland, as well as in laboratory trials. In the laboratory,
we challenged P. subordinaria strains with Plantago
lanceolata latent virus (PlLV) in order to understand how cross-kingdom
interactions affect within-host infection load and transmission
potential, as well as their potential trade-off. Specifically, we ask 1)
How common is P. subordinaria in the Åland Islands, and is there
natural variation in within-host infection load in natural P.
lanceolata populations, and 2) Is there a trade-off between within-host
infection load and population size (potential proxy for among-host
natural transmission) in P. subordinaria ? We hypothesize that
high within-host infection load comes with a cost of lower transmission,
measured as pathogen population size. In a laboratory experiment, we
tested: 3) Is there a trade-off between laboratory measured within-host
infection load and transmission potential of P. subordinaria ? We
hypothesize that high within-host infection load is costly with respect
to transmission potential. 4) Does coinfection with PlLV alter P.
subordinaria within-host infection load and transmission potential? We
hypothesize that coinfection increases both within-host infection load
and transmission potential.